Dermatology: Practical and Conceptual Review | Dermatol Pract Concept. 2024;14(4):e2024270 1 Dupilumab and Alopecia Areata: A Possible Combined or Disturbance Therapy? A Review of The Literature Michela Starace1,2, Stephano Cedirian1,2, Federico Quadrelli1,2, Francesca Pampaloni1,2, Tullio Brunetti1,2, Marco Adriano Chessa1,2, Carlotta Gurioli1, Bianca Maria Piraccini1,2, Iria Neri1 1 Dermatology Unit, IRCCS Azienda Ospedaliero-Universitaria di Bologna, Policlinico S. Orsola-Malpighi, Bologna, Italy 2 Department of Medical and Surgical Sciences, Alma Mater Studiorum University of Bologna, Italy Key words: Dupilumab, Th1-inflammation, Th2-inflammation, Alopecia areata, Atopic dermatitis Citation: Starace M, Cedirian S, Quadrelli F, et al. Dupilumab and Alopecia Areata: A Possible Combined or Disturbance Therapy? A Review of The Literature. Dermatol Pract Concept. 2024;14(4):e2024270. DOI: https://doi.org/10.5826/dpc.1404a270 Accepted: June 21, 2024; Published: October 2024 Copyright: ©2024 Starace et al. This is an open-access article distributed under the terms of the Creative Commons Attribution- NonCommercial License (BY-NC-4.0), https://creativecommons.org/licenses/by-nc/4.0/, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original authors and source are credited. Funding: None. Competing Interests: None. Authorship: All authors have contributed significantly to this publication. Corresponding Author: Bianca Maria Piraccini MD, PhD, Via Massarenti 1, 40138 Bologna Italy. telephone: +390512144840. Email: biancamaria.piraccini@unibo.it Introduction: Dupilumab, a monoclonal antibody targeting IL-4 receptor subunit alpha, treats atopic dermatitis (AD) and may impact alopecia areata (AA). AA involves Th1-driven immune activity, and recent studies suggest a role for Th2 pathways. Dupilumab’s effects on AA are mixed, with reports of both improvement and worsening. Objectives: This study aims to review the effects of dupilumab on AA in patients with AD, analyzing literature to understand cases of improvement or worsening and identifying contributing factors. Methods: A literature review was conducted using articles in platforms such as PubMed, Scopus, and Web of Science written up to April 2024, focusing on studies involving AA, AD, and dupilumab. Articles were analyzed for patient demographics, disease characteristics, and responses to treatment. Results: Out of 35 articles reviewed, 13 AA cases worsened after dupilumab (mean age 32.8; mostly males with patchy alopecia), and 38 cases showed improvement (mean age 27.6; majority females, varying AA types). Full hair regrowth occurred in 11 improved cases, while 9 had partial regrowth. Conclusions: Dupilumab shows dual effects on AA, influenced by Th1/Th2 immune profiles. Worsening was more common in males with Th1-driven AA, while females with Th2-skewed AA saw improvement. Factors like age, disease severity, and IgE levels may affect outcomes, suggesting a need for personalized treatment approaches for AA patients with AD. ABSTRACT 2 Review | Dermatol Pract Concept. 2024;14(4):e2024270 Introduction Dupilumab is a monoclonal antibody that targets IL-4 re- ceptor subunit alpha (IL-4R-alpha), a shared component of IL-4 and IL-13 receptors; these cytokines have a pivotal role in Th2-driven inflammation. Dupilumab has been approved for the treatment of moderate-to-severe atopic dermatitis (AD) however, recently, it has shown efficacy in other condi- tions, such as alopecia areata (AA) [1]. AA is an autoimmune non-scarring alopecia that can affect any hair-bearing area. The (IFN)y/Th1 pathway and the Janus kinase (JAK) signal- ing pathway are the main protagonists of hair follicle im- mune aggression in AA, although recent studies have shown a co-participation of Th2-axis cytokines [2]. The possible association between AD and AA has already been published, and for this reason, many cases have been described about the use of dupilumab in patients with both dermatological diseases [3]. The literature shows that dupi- lumab may have a double effect on patients affected by AA and AD: it has been reported that it may promote AA devel- opment as well as hair re-growth, something that could be related to a specific pattern of cytokines associated with AA inflammatory background [4,5]. Objectives We conducted a literature review to define the different ef- fects of dupilumab in patients with AA. More specifically, we wanted to review the current literature on the topic so as to understand any proven relationship between dupilumab ad- ministration and improvement/worsening of AA in patients with AD. Furthermore, to the best of our knowledge, we wanted to report all the similar cases that could strengthen such duality in dupilumab use. Lastly, we wanted to analyze the data found and draw conclusions on the topic, based on the existing evidence, as previously stated. Methods We performed a literature review using the medical databases PubMed, Scopus, and Web of Science. We included keywords “dupilumab”, “alopecia areata”, and “atopic dermatitis”. We included articles written up to April 2024. Selected ar- ticles were based on relevance, focusing on case reports, reviews, and original articles. Articles that did not provide relevant information or were not written in English were excluded. Subsequently, we collected all data on patients demographic characteristics, disease profile, and personal response to dupilumab. Finally, we divided our findings into two different categories based on how dupilumab affected AA patients (Tables 1 and 2). Results Our review of the literature yielded important findings re- garding the dual efficacy of dupilumab in patients affected with AA and AD. We found and analyzed a total of 35 rele- vant articles (Tables 1 and 2). Among these, 13 cases of AA worsened after dupilumab (M = 8; F = 5; Mean Age = 32.8), whilst 38 cases of AA improved after dupilumab (M = 18; F = 20; mean age = 27.6). The clinical characteristics of AA in patients who wors- ened after starting dupilumab were mostly of a patchy alo- pecias (n = 9), with three diffuse forms and one case of AA in androgenetic alopecia pattern. Six patients had complete regrowth after discontinuation of dupilumab, whilst three patients had only partial regrowth. Two patients were still under treatment at the moment of the publication of the studies, and two patients had no information about AA evo- lution after the modification of dupilumab therapy (Table 1). Regarding the cohort of patients that experienced hair regrowth after starting dupilumab, eleven patients had al- opecia areata universalis (AAU), nine patients had alopecia areata totalis (AAT), three patients had alopecia areata sub- totalis (AA with a SALT score greater than 80% and less than 100%), and 15 patients had a patchy alopecia. Eleven patients were associated with full regrowth, whereas nine patients reported partial regrowth (one of them had a wors- ening of AA partial regrowth after dupilumab suspension) (Table 2). Discussion The results of our literature review provide interesting in- sights into the dual impact of dupilumab on patients affected by AA and AD. We reviewed 35 relevant articles exploring the relationship between these conditions and the role of dupi- lumab (Tables 1 and 2). Our analysis revealed that 13 cases of AA worsened after starting dupilumab, whereas 38 cases of AA showed improvement (Tables 1 and 2). This show- cases how the efficacy of dupilumab in AA can be variable, likely due to individual factors. Patients who experienced a worsening of their condition were predominantly male, with patchy alopecia. The worsening typically began around 17 weeks after starting the drug; however, some of these patients experienced hair regrowth after discontinuing dup- ilumab (Table 1). On the other hand, patients who showed improvement in AA after starting dupilumab were mostly fe- male, with a broader range of severity (from patchy alopecia to AAU). A significant number of these patients experienced full hair regrowth, suggesting that dupilumab could help promote hair regrowth in specific AA cases (Table 2) [6-36]. Dupilumab provides a distinct perspective on the inter- play between AA and AD. The literature suggests that this Review | Dermatol Pract Concept. 2024;14(4):e2024270 3 drug can have a dual effect on these conditions, possibly due to its suppression of Th2-axis inflammation [6-36]. On this matter, recent research indicates that AA may be linked to two distinct pathogenetic pathways: a Th1-skewed and a Th2-skewed mechanism [3]. The existence of two different pathways may explain the opposing responses to dupilumab observed in AA patients. In individuals with Th2-skewed AA, inhibiting Th2 inflammation with dupilumab can lead to hair regrowth. However, for patients with Th1-skewed AA, dupilumab-induced suppression of Th2 may exacer- bate Th1-driven inflammation, resulting in hair loss [37-39]. Additionally, Marks et al. observed that female patients are more likely to have a Th2-skewed condition, while males are more often associated with a Th1-skewed condition. This is also demonstrated by our data, as the cohort of patients who improved were predominantly female (Th2-skewed), and those who worsened were mostly male (Th1-skewed) [37]. Future research could focus on better identifying the underlying pathogenic mechanism in AA patients, leading to patient-tailored treatment. Dupilumab has shown efficacy in treating AA in children (< 18 years old); indeed, as displayed in our dataset, 16 chil- dren experienced hair regrowth after taking dupilumab, while only McKenzie et al. reported two patients with worsening Table 1. Cases of AA Worsening after Dupilumab. No of patients Sex (M/F) Age Clinical characteristics of AA/onset after dupilumab Clinical course after steroid treatment/CyA/dupilumab discontinuation Reference 1 M 29 AA in patches – 5 weeks Partial regrowth (undergoing treatment at the moment of the publication of the article) Mitchell K et al. (2018) 1 M 31 AA in patches on the anterior scalp – 6 weeks Undergoing treatment at the moment of the publication of the article Barroso-Garcia et al. (2018) 1 M 33 Diffuse AA in the frontal and occipital region + beard – 7 weeks Complete hair regrowth after 3 months Salguero- Fernandez et al. (2018) 1 M 24 AA in patches – 1 week Partial regrowth after 3 weeks (ketoconazole 3% shampoo was used) Yazdanyar S et al. (2019) 1 F 23 AA in patches in the frontal, vertex and occipital areas – 48 hours Complete regrowth after 6 months (dupilumab was discontinued) Barbarin C et al. (2019) 1 M 27 AA in the vertex and temporal areas – 18 weeks Complete regrowth after 2 months (dupilumab was discontinued) Flanagan K et al. (2019) 1 M 35 AA in patches, mostly in the parietal, occipital and frontal regions – 6 weeks Partial regrowth (78%) after 4 months Kanda N et al. (2019) 1 M 53 AA in patches – 1 year Complete regrowth after 4 months (dupilumab was discontinued, and Cya was started) Stander S et al. (2020) 1 F 42 AA in androgenetic alopecia pattern – 4 months Complete regrowth after 2 months Carnicle J et al (2021) 1 F 45 AA in oval patches in the occipital region + two small patches in the temporal region – 1 year Complete hair regrowth after 2 months Beaziz J et al. (2021) 2 F = 2 16.5 (mean age) Mean SALT = 91.5 1 patient reached SALT 100 (starting from SALT98 after 5 months of therapy); the other patient reached SALT98 (starting from SALT85 after 2 months of therapy). McKenzie et al. (2021) 1 M 36 AA of the beard – 25 weeks Information not available in the article Chromy D et al. (2023) 4 Review | Dermatol Pract Concept. 2024;14(4):e2024270 Ta b le 2 . C as es o f A A I m pr ov ed a ft er D up ilu m ab . N o o f p at ie n ts Se x (M /F ) A g e (y ea rs ) B as el in e cl in ic al c h ar ac te ri st ic s C lin ic al C o u rs e af te r D u p ilu m ab o n se t R ef er en ce 1 F 13 A A T R eg ro w th o n 60 % o f sc al p Pe nz i L R e t al . ( 20 18 ) 1 F 49 A A U Fu ll re gr ow th a ft er 8 m on th s A ln ie m i D T e t al . ( 20 18 ) 1 M 28 A A s ub to ta lis ( SA LT s co re 8 7, 4) in a n A D p at ie nt (E A SI s co re : 1 4. 9 - Ig E = 1 1. 98 7 IU /m L ) Fu ll re gr ow th a t m on th 6 a nd A D s co re s w er e si gn ifi ca nt ly re du ce d (E A SI s co re : 6 .5 ) D ar ri ga de A -S e t al . (2 01 8) 1 F 35 A A U Fu ll re gr ow th a ft er 1 2 m on th s Sm og or ze w sk i J e t al . (2 01 9) 1 F 25 A A T A lm os t fu ll re gr ow th a ft er 1 1 m on th s A sz od i N e t al . ( 20 19 ) 2 M - M 38 - 3 2 A A U – A A w it h op hi as is p at te rn Fu ll re gr ow th – f ul l r eg ro w th L ud ri ks on e L e t al . (2 01 9) 1 M 44 A A in f oc al p at ch es ( SA LT 6 1. 6) in a n at op ic de rm at it is p at ie nt ( E A SI s co re : 4 6. 7 - Ig E = 4 43 00 I U /m L ) A lm os t fu ll re gr ow th a nd im pr ov em en t of t he s ki n m an if es ta ti on s (i n 3 m on th s E A SI s co re : 2 5) U ch id a H e t al . ( 20 19 ) 1 M 49 A A in f oc al p at ch es Fu ll re gr ow th a ft er 3 m on th s M ag da le no -T ap ia l J et a l. (2 01 9) 1 F 33 A A in p at ch es c om pl ic at ed w it h tr ic ho ti llo m an ia in a n at op ic d er m at it is p at ie nt ( E A SI s co re : 4 6) A lm os t co m pl et e re gr ow th a ft er 1 9 w ee ks . T he p at ie nt ’s sk in c on di ti on h ad a ls o im pr ov ed ( E A SI s co re : 9 .6 ). U sh id a M e t al . ( 20 20 ) 7 F = 2; M = 5 40 ( m ea n ag e) M ea n SA LT = 7 9. 2 (M ea n E A SI = 3 9. 93 ; M ea n Ig E = 1 07 94 .7 U I/ m L ) M ea n SA LT o f 28 .5 a ft er t re at m en t - m ed ia n du ra ti on of 2 4 w ee ks ) H ar ad a K e t al . ( 20 20 ) 1 F 13 A A T Fu ll re gr ow th a ft er 4 m on th s (m in im al e ye la sh a nd e ye br ow re gr ow th ) G ru en st ei n D e t al . (2 02 0) 1 F 34 A A U C om pl et e re gr ow th o f co ur se t er m in al h ai r on t he s ca lp , fa ce , f or ea rm s, p ub ic a re a, a nd le gs a ft er 1 0 m on th s C al l J E e t al . ( 20 20 ) 1 F 30 A A T in a n at op ic d er m at it is p at ie nt ( E A SI s co re : 3 6) C om pl et e re gr ow th a ft er 3 m on th s an d an im pr ov em en t in A D ( E A SI s co re : 9 .6 ) Sz ek el y S et a l. (2 02 0) 1 F 21 A A U Pa rt ia l r eg ro w th w it h a si ng le p at ch le ft a ft er 4 m on th s A lo ta ib i e t al . ( 20 21 ) Review | Dermatol Pract Concept. 2024;14(4):e2024270 5 5 M = 3 ; F = 2 12 .8 (m ea n ag e) 57 ( m ea n SA LT ) 1 pa ti en t w en t fr om S A LT 25 t o SA LT 0 af te r 12 m on th s of t he ra py ; 1 p at ie nt w en t fr om S A LT 35 t o SA LT 8 af te r 7 m on th s of t he ra py ; 1 p at ie nt w en t fr om S A LT 10 0 to SA LT 98 a ft er 1 2 m on th s of t he ra py ; 1 p at ie nt w en t fr om SA LT 10 0 to S A LT 50 a ft er 1 1 m on th s of t he ra py ; 1 p at ie nt w en t fr om S A LT 25 t o SA LT 0 af te r 12 m on th s of t he ra py . M cK en zi e et a l. (2 02 1) 1 F 46 A A U Pa rt ia l r eg ro w th o f th e fa ce , s ca lp , a nd lo w er le gs R ei nh ol d L e t al . ( 20 22 ) 1 M 16 A A T C om pl et e re gr ow th a ft er 3 y ea rs K ul ka rn i M e t al . ( 20 22 ) 5 M = 2 ; F = 3 4. 6 (m ea n ag e) M ea n SA LT = 6 0. 8 4 pa ti en ts r ea ch ed S A LT 0 , a nd 1 p at ie nt r ea ch ed S A LT 20 . (N o ti m e- of -t re at m en t is g iv en f or t he 5 p at ie nt s) . T hr ee ou t of 6 w er e si m ul ta ne ou sl y tr ea te d w it h or al m in ox id il + to pi ca l t of ac it in ib , t op ic al m in ox id il + to pi ca l t of ac it in ib an d pu ls ed p re dn is on e + or al m in ox id il, r es pe ct iv el y. C ho e t al . ( 20 23 ) 1 F 9 A A s ub to ta lis - S A LT s co re 9 8 (I gE = 9 99 .6 I U /m L ) H ai r re gr ow th , t og et he r w it h re pi gm en ta ti on o f re gr ow n w hi te t er m in al h ai r de n ov o w it ho ut d is tu rb in g th e an ag en ph as e of h ai r fo lli cl es . Y an X e t al . ( 20 23 ) 1 F 4 A A U Pa rt ia l r eg ro w th o f th e ha ir ; e ye br ow s an d ey el as he s fu lly re st or ed C ai L e t al . ( 20 23 ) 1 F 45 A A U R eg ro w th a ft er 6 m on th s (i t is n ot s pe ci fie d in t he a rt ic le if pa rt ia l o r co m pl et e re sp on se ) M cF ee ly O . ( 20 23 ) 1 M 1 A A U Pa rt ia l r eg ro w th Ta nc re di V e t al . ( 20 24 ) 1 M 12 A A w it h op hi as is p at te rn C om pl et e re gr ow th a ft er 2 m on th s G ua ld i G e t al . ( 20 24 ) 6 Review | Dermatol Pract Concept. 2024;14(4):e2024270 alopecia areata. Exp Dermatol. 2020;29(8):726-732. DOI:10.1111 /exd.14129. 4. Renert-Yuval Y, Guttman-Yassky E. The Changing Landscape of Alopecia Areata: The Therapeutic Paradigm. Adv Ther. 2017;34(7):1594-1609. DOI:10.1007/s12325-017-0542-7. 5. Shohat M, Mimouni D, Ben-Amitai D, et al. In vitro cytokine profile in childhood alopecia areata and the immunomodula- tory effects of AS-101. Clin Exp Dermatol. 2005;30(4):432-434. DOI:10.1111/j.1365-2230.2005.01817.x. 6. Mitchell K, Levitt J. Alopecia areata after dupilumab for atopic dermatitis. JAAD Case Rep. 2018;4(2):143-144. DOI:10.1016 /j.jdcr.2017.11.020. 7. Barroso-García B, Rial MJ, Molina A, Sastre J. Alopecia Areata in Severe Atopic Dermatitis Treated With Dupilumab. J Investig Allergol Clin Immunol. 2018;28(6):420-421. DOI:10.18176/jiaci .0301. 8. Salgüero-Fernández I, Gonzalez de Domingo MA, Suarez D, Roustan-Gullón G. Dermatitis and alopecia in a patient treated with dupilumab: a new adverse effect? Clin Exp Dermatol. 2019;44(3):e41-e43. DOI:10.1111/ced.13858. 9. Yazdanyar S, Jemec GBE. Alopecia Areata After Treatment with Dupilumab. Dermat Contact Atopic Occup Drug. 2019; 30(2):175-176. DOI:10.1097/DER.0000000000000458. 10. Barbarin C, Hosteing S, Nosbaum A, Allouchery M, Celerier P. Early onset of alopecia areata after dupilumab introduc- tion in a patient with atopic dermatitis. Eur J Dermatol EJD. 2019;29(5):542-543. DOI:10.1684/ejd.2019.3626. 11. Flanagan K, Sperling L, Lin J. Drug-induced alopecia after dupi- lumab therapy. JAAD Case Rep. 2019;5(1):54-56. DOI:10.1016 /j.jdcr.2018.10.010. 12. Kanda N, Koto M, Hoashi T, Saeki H. Case of alopecia areata during dupilumab treatment for atopic dermatitis. J Dermatol. 2019;46(9):e332-e333. DOI:10.1111/1346-8138.14880. 13. Ständer S, Trense Y, Thaçi D, Ludwig RJ. Alopecia areata devel- opment in atopic dermatitis patients treated with dupilumab. J Eur Acad Dermatol Venereol JEADV. 2020;34(10):e612-e613. DOI:10.1111/jdv.16493. 14. Carnicle JM, Hendricks AJ, Shi VY. Reactivation of Alope- cia Areata After Dupilumab Therapy for Atopic Dermatitis. Dermat Contact Atopic Occup Drug. 2021;32(1S):e80-e82. DOI:10.1097/DER.0000000000000512. 15. Beaziz J, Bouaziz JD, Jachiet M, Fite C, Lons-Danic D. Dupilumab-induced psoriasis and alopecia areata: Case report and review of the literature. Ann Dermatol Venereol. 2021; 148(3):198-201. DOI:10.1016/j.annder.2021.02.003. 16. Penzi LR, Yasuda M, Manatis-Lornell A, Hagigeorges D, Senna MM. Hair Regrowth in a Patient With Long-standing Alopecia Totalis and Atopic Dermatitis Treated With Dupilumab. JAMA Dermatol. 2018;154(11):1358-1360. DOI:10.1001 /jamadermatol.2018.2976. 17. Smogorzewski J, Sierro T, Compoginis G, Kim G. Remission of alopecia universalis in a patient with atopic dermatitis treated with dupilumab. JAAD Case Rep. 2019;5(2):116-117. DOI:10.1016 /j.jdcr.2018.11.007. 18. Darrigade AS, Legrand A, Andreu N, et al. Dual efficacy of dupi- lumab in a patient with concomitant atopic dermatitis and alope- cia areata. Br J Dermatol. 2018;179(2):534-536. DOI:10.1111 /bjd.16711. 19. Alniemi DT, McGevna L. Dupilumab treatment for atopic dermatitis leading to unexpected treatment for alopecia conditions [38]. This is consistent with prior reports that link such variability to severe and/or long-standing AA [37]; in- deed, these variants seem to be related to a higher chance of improvement after dupilumab administration. Additionally, it seems that dupilumab is associated with a slow onset of ac- tion in children and works better when combined with other therapies such as oral minoxidil [38,39]. Lastly, another factor that may be linked to the varying response to dupilumab in AA patients could be IgE levels. Indeed, Guttman-Yassky et al. conducted a Phase 2a clinical trial and noted that progress rates were higher in patients with baseline IgE levels of 200 IU/ml or more, demonstrating how a Th2-directed therapy could be beneficial for specific AA patients [1]. Although not many articles in our review reported IgE levels, all patients with high IgE levels improved significantly, which aligns with the literature [1]. We identified two potential limitations of this study that we would like to state. The first is represented by a possible selection bias due to a greater propensity to publish positive results of dupilumab on alopecia areata. The second is the absence of an indication for dupilumab for alopecia areata, making its use more difficult in patients affected solely by alopecia areata. 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